BIODIVERSITAS ISSN: 1412-033X Volume 19, Number 2, March 2018 E-ISSN: 2085-4722 Pages: 591-603 DOI: 10.13057/biodiv/d190230

Diversity, potential and conservation of in Bogor Botanic Gardens, Indonesia

TRI HANDAYANI Center for Conservation, Indonesian Botanic Gardens (Bogor Botanic Gardens), Indonesian Institute of Sciences. Jl. Ir. H. Juanda No. 13 Bogor 16122, West Java, Indonesia. Tel.: +62-251-8322187, Fax.: +62-251-8322187, email: [email protected]

Manuscript received: 4 December 2017. Revision accepted: 16 March 2018.

Abstract. Handayani T. 2018. Diversity, potential and conservation of Annonaceae in Bogor Botanic Gardens, Indonesia. Biodiversitas 19: 591-603. The Annonaceae is a large family of trees, shrubs and climbers consisting of about 109 genera and 2440 . This family has important economic value for fresh , cosmetics and perfumes, timber, traditional medicines, processed foods and beverages, insecticides, and ornamental . It also has an important role in forest ecosystems and in environmental management, as a key habitat organism. Despite its many uses, the family has not received special attention, and many of its species have been forgotten. Therefore, efforts are required to conserve the Annonaceae. Conservation of the Annonaceae depends upon ex-situ as well as in-situ methods. Conservation by ex situ approaches is considered effective because it can save from extinction species that are rare, endemic or of as yet recognized, unknown usefulness.The research reported in this paper aimed to determine Annonaceae diversity in Bogor Botanic Gardens (BBG), West Java, Indonesia as well as its current and potential utilization, with a view to developing ways of ensuring preservation of the collection within the Gardens. The study used direct observation of the Garden’s collection, compilation and scrutiny of relevant data from the long-term BBG registration database, analysis of past research data, and a literature study. Currently, BBG holds in its collection about 28 genera and 83 species of the Annonaceae family. The collection is estimated to cover 80% of the total species scattered across the Malesian region. Within the collection there are 49 tree species (59.04%), 14 shrub species (16.87%) and 20 liana species (24.09%). Most of the collections are from Java and Sumatra, while the fewest are from Maluku Islands and Papua. Among 40 species observed, 7 species are used for their fruit, 7 species have cosmetic or perfume uses, 22 species are a source of timber, 34 species have uses in traditional medicine, 6 species are used in the food or beverage industry, 19 species can be used as ornamental plants, 8 species for insecticides, and 4 species for other uses.The Annonaceae collections consist of young and old plants.Plants within the Gardens that are more than 100 years old include trees (7 species), shrubs (3 species) and a liana (1 species).The most widely used parts for traditional medicine are roots and leaves. This paper discusses the efforts taken by BBG to conserve the Annonaceae, include maintaining the diversity of the collection, researching the potential usefulness of the collection and exploring different approaches to its conservation.

Keywords: Annonaceae, collection, conservation, research, potential

INTRODUCTION and Akpapan 2012; Uyoh et al. 2013; Handayani 2016); timber (Nurfadilah et al. 2017); traditional medicines The human population of Indonesia continues to (Wang et al. 2002; Blessing et al. 2010; Purwantiningsih et increase from year to year. Increasing populations cause al. 2011; Wang et al. 2012; Rosandy et al. 2013; Biba et al. environmental problems due to over-exploitation of land, 2014; Enabulele et al. 2014); processed foods and expansion of plantations, and deforestation (Nagel 2011). beverages (Bele et al. 2011; Akpabio and Akpapan 2012; These activities have caused destruction of forests as Eze-Steven et al. 2013; Tatdao et al. 2014); ornamental habitats for flora and fauna. Forest destruction also causes plants (Handayani 2016; Handayani 2017); pesticides (Bele the loss of species that are known to the public, or et al. 2011; Cheng et al. 2012); and other comodities unknown and hence not available for potential utilization. (Wakhidah et al. 2017). Members of the Annonaceae play In order to prevent the possible flora extinction in the wild, an important ecological role in terms of species diversity, such as particular species of the family Annonaceae, especially in tropical rainforest ecosystems (Couvreur et al. conservation efforts are being undertaken at sites outside 2012). However, the Annonaceae populations in natural the flora’s natural habitats (ex situ conservation), such as in habitats continue to be threatened. Pressures on forest in the facilities of Bogor Botanical Gardens (BBG) in West the form of exploitation for forest products, and of Java, Indonesia. conversion to agricultural land, plantations, housing and The Annonaceae is a large family of trees, shrubs, and mining land occur continuously (Yusuf et al. 2005; Komara climbers, which occurs in tropical and subtropical regions. et al. 2016). Harvesting Annonaceous plants from the It consists of about 109 genera and 2440 species (Couvreur forest, as a source of timber or raw material for traditional et al. 2012). Economically, the family is important as a medicine is a direct cause of population decline of source of edible (Aziz et al. 2016);cosmetics and particular species. This affects the balance of the forest perfumes (Leboeuf et al. 1982; Bele et al. 2011, Akpabio ecosystem. 592 BIODIVERSITAS 19 (2): 591-603, March 2018

Bogor Botanical Gardens is located in Bogor city, West Observations on the diversity of Annonaceae Java Province, Indonesia. As an ex-situ plant conservation Only plants that have been identified to species level institution, BBG plays important roles in preventing plant were observed as part of the assessment of diversity. Forty species extinction. Apart from this, the existence of BBG in species of trees, shrubs and lianas were used as observation the middle of downtown Bogor makes a very important samples. Observations focused on variation in species, contribution to the tackling of environmental problems in plant habit, flower color, coloration of new foliage, Bogor city and its surroundings.The Annonaceae is one of specimen origin, habitat, and reproductive traits. the families in the plant collection of BBG with a Observations were made by naked eye, camera, and particularly large number of species represented. The microscope. The size of trees was classified as small if the Annonaceae play an important role in the artificial forest had a high < 5 m and large trees were those with a high > 5 ecosystem of the Gardens. The plants have ecological, m. The floral diameter was measured with a ruler: flowers hydrological, and climatological functions. Many members were classified as small if they had a diameter < 2 cm; of the collection are large enough to represent significant medium flowers were 2-5 cm in diameter, and large carbon sinks within the ecosystem (Didi Usmadi, pers. flowers were those with a diameter > 5 cm. com.). They also contribute to the oxygen balance and provide habitats for other organisms. The loss of Observation of recent research activity conducted on Annonaceae in the wild and BBG would have impacts on Annonaceae the balance of these ecosystems and human life dependent The research reported here summarises all research on them. It is therefore essential that concerted efforts be recently carried out on the Annonaceae collection of BBG; taken both in the wild and within the BBG ex-situ this includes research done in greenhouses, in the open conservation facility, to provide for the preservation of the garden, and reported in published literature. All research family Annonaceae and the sustainability of their relating to is generally carried out in a greenhouse. utilization by human society (Sari et al. 2005;Yusuf et al. Observations on reproductive aspects of the growing plants 2005; Nagel 2011; Couvreur et al. 2012; are conducted in the open gardens. Observations on insect The conservation of the Annonaceae involves both in visitors were carried out on 15 flowering plants.This study situ and ex-situ approaches. In situ conservation is indirect, also reviewed other research that was conducted at BBG. since the goal to protect the Annonaceae is not specific. In situ conservation focuses on species that grow in protected Observation of the potential uses of Annonaceae forest, national parks, indigenous forest, nature parks and Observations were made on 40 species in the BBG nature reserves (Hartini and Puspitaningtyas 2009). Ex situ plant collection. Observations of the potential uses of the conservation aims to preserve the Annonaceae directly plant were carried out directly, and included recording within botanical gardens, city forests, city parks, arboreta interesting aspects of the plants, such as the color of and community plantations. Due to its ability to preserve flowers, the color of young leaves, and the stature of trees. species that are rare, endemic or of unknown benefits, this Furthermore, interviews and information from the literature method is considered more effective in preventing were also used as source data. extinction of targeted species. This study aimed to: (i) determine the diversity of the Observation of the conservation of Annonaceae Annonaceae as represented in Bogor Botanic Gardens, (ii) Observations were conducted on conservation activities record the results of previous research carried out into related to the technical preservation of plant members of Annonaceae at BBG, (iii) explore the potential of the the Annonaceae. In situ conservation, location data were Annonaceae for utilization by society, and (iv) study the obtained from the literature. Data relating to technical ways to conserve the family’s diversity. aspects of plant conservation were collected from technicians working in BBG. Data relating to the collection were also observed directly and obtained from the MATERIALS AND METHODS Registration and Nursery Sub-Divisions.

Time and place Data analysis This research was carried out at Bogor Botanic Gardens The data on plant origins, number of species based on (BBG), Bogor, West Java, Indonesia between 2014 and ages cultivated in BBG and useful parts of the plant were 2016. The altitude of BBG is about 260 m asl, relative collated and analyzed using an MS Excel spreadsheet. humidity is 34-80 %, and temperature varies between 25- 39°C. RESULTS AND DISCUSSION Plant materials This research used the collection of Annonaceae in Diversity of Annonaceae in Bogor Botanical Gardens BBG as the study material. Data on the Annonaceae Table 1 summarizes the types of data collected on the members of the Gardens were compiled from the diversity of Annonaceae in BBG, including information Registration and Nursery Sub-divisions of BBG as well as about plant species, plant origins, habit, plants age, growth from a review of the published literature. site, reproduction traits, young leaf color, and flower color. Based on the catalog of “An Alphabetical List of Plant

HANDAYANI – Annonaceae in Bogor Botanical Gardens 593

Species Cultivated in The Bogor Botanic Gardens” (Sari et Plants habitus al. 2010), 83 species belonging to 28 genera have been The growth habit of Annonaceae members varies; identified in the Annonaceae collection.The collection is i.e.trees, shrubs or lianas. At BBG, the Annonaceae estimated to hold plants belonging to 80% of the total collection is composed of 49 species of tree (59.04%), 14 species scattered in the Malesian region. The number of species of shrub (16.87%) and 20 species of liana (24.0%). species per varies from one to 11 species. The greatest numbers of tree species are in the Anomianthus, Dasymaschalon, , Enicosanthum, genus. Most of the shrubs are from the genera Annona and , Platymitra, Saccopetalum, and Xylopia, are Goniothalamus.The members of the genus Uvaria are genera consisting of just one species. Polyalthiais the mostly liana. The size of the trees in Annonaceae family genus with the most number of species, i.e., 11 species. rang from small to large. Small tree There are ten species of large trees, i.e., , Table 1. Characteristics of Annonaceae plants in Bogor Botanic sumatranus, C. martabanicus, , Mezzettia Gardens, West Java, Indonesia parviflora, Monodora myristica, Polyalthia glauca, P.lateriflora, Platymitra macrocarpa, Characteristic Recorded states of characteristic burahol, and Xylopia aethiopica. documented Origins of the plants Indonesia; foreign Habitus Tree; shrub; and liana Origin of the plants Age of plants Young; old The collection of Annonaceae in BBG comes from The growth site Shaded; slight shade; and open area various regions of Indonesia and foreign introductions. The Flowering and fruiting Seasonal; simultaneous largest number of plants in the collection is from Java and season Sumatra, while the fewest are from Maluku and Papua Flowering type Flushing; not flushing (Figure 1). Because the amount of exploration conducted Flowering pattern Once a year; continuously on the islands of Java and Sumatra has been greater than in The size of flower Small; medium; and large Maluku and Papua, so the possibility of obtaining The color of young leaf Greenish-brown, pink, and yellowish- green collections has also been greater. In addition, the diversity The color of flower White, red, purplish-red, green, of all flora collections in BBG from Java and Sumatra is purplish-green, yellow, reddish- higher than from Maluku and Papua. yellow, brown, and reddish-brown Age of plants The Annonaceae collection of BBG consists of both

young and old plants. Based on my observation of 40 sample species one specimen per species) and results of data analysis from the BBG Registration section, the plants specimen of 13 species are still young (< 25 years), 21 species are more than 50 years old, 11 species are more than 100 years and a plant of one species is more than 150 years old (Figure 2). The plants which more than 100 years

Percentageof plant(%) old are from seven species of trees, three species of shrub

and one species of liana.The oldest tree in the Annonaceae

Java collection, a specimen of Platymitra macrocarpa, is 173 Papua Foreign Sumatra

Sulawesi years of age; it was planted in BBG in 1844. The oldest Moluccas Kalimantan L. Isl. Sunda shrub, a specimen of Goniothalamus macrophyllus, 120 Plants origin years old, was planted in 1897. One plant belonging to the Figure 1. The origins of Annonaceae plants in the collection of species Uvaria rufa at 118 years of age is the oldest liana in Bogor Botanical Gardens, West Java, Indonesia the Annonaceae collection. It was planted in BBG in 1899.

Leaf and flower colors The color of young leaves of Annonaceae varies, i.e.

greenish-brown, pink, and yellowish-green (Figure 3.A, 3.B, 3.C). Species whose young leaves are pink include number

s s Stelechocarpus burahol, fruticosum, and Polyalthia lateriflora, whereas, Saccopetalum horsfieldii, Plant Monodora myristica and Polyalthia rumphii have young leaves that are yellowish-green. Plants with greenish-brown young leaves can be found in the species Goniothalamus macrophyllus and Meiogyne virgata. The size of flowers of Annonaceae species in BBG varies from small to large. Plants age From the 40 species sampled, 15 plants had small flowers, Figure 2. The total number of species in the Annonaceae family 15 had medium-sized flowers and 10 had large flowers. of Bogor Botanical Gardens, West Java, Indonesia, classified Platymitra macrocarpa flowers are the smallest in size, according to the age of the plant specimen in the collection

594 BIODIVERSITAS 19 (2): 591-603, March 2018 while the flowers of Monodora myristica have the largest found in flowers of Monodora myristica (Figure 3.D), size. The color of the Annonaceae flowers also varies. The Polyalthia lateriflora (Figure 3.H), or Mitrephora color variations found are white, red, purplish-red, green, polypyrena (Figure 3G). Sometimes, the color of the purplish-green, yellow, reddish-yellow, brown, and flowers will change with the age of the flowers. For reddish-brown.The most common color found is yellow. example, when the flower of Mitrephora polypyrena Flower color can be single (one color) or mixed (more than blooms its outer petal is white (Figure 3.G) but then turns one color). Single colored flowers can be found in the to yellow. Flower color is an important visual cue for most species Cananga odorata (Figure 3.E), Cyathocalyx pollinators (Johnson and Dafni 1998). martabanicus and Polyalthia rumphii. Mixed colors can be

A B C

D E F

G H I

Figure 3. The color of young leaves, and flowers of Annonaceae plant species. A. Goniothalamus macrophyllus young leaves, B. Stelechocarpus burahol young leaves, C. Polyalthia rumphii young leaves D. Monodora myristica flower, E. Cananga odorata flower, F. Uvaria hirsuta flower, G. Mitrephora polypyrena flower, H. Polyalthia lateriflora flower, I. Alphonsea teysmannii flower. 3.A-C scales = 2 cm; 3.D-I scales = 1 cm

HANDAYANI – Annonaceae in Bogor Botanical Gardens 595

Growth site of the plants burahol. The successful fruiting of a species is influenced The environment of the growth sites of the Annonaceae by visiting insects, especially pollinators. Some of the in the BBG collection varies, from shady locations, to visiting insects are suspected of being pollinators, because slightly shaded, to open locations. These differences in their feet were observed to be carrying pollen from one location cause differences in growth and development of flower to others. According to Goodrich (2012) and the plants. Plants in shaded places grow poorly, with Saunders (2012) there are five groups of Annonaceae incomplete branching, susceptibility to disease, and flower pollinators namely beetles, bees, flies, mites and difficulty in flowering and fruiting. Plants in open areas cockroaches. On the other hand, in BBG, cockroaches have have healthier, stronger growth, perfect branching and never been recorded visiting flowers of Annonaceae. often produce flowers and fruit. Initially, specimens of Sometimes there is a symbiosis between plants and visiting Annonaceae collected from exploration trips are planted insects such as weaver ants with Polyalthia rumphii. insufficient light in BBG. Some vigorous species grow fast Symbiosis between ants and Annonaceae plants in BBG and large so that they are not overshadowed by other also occur in Polyalthia lateriflora, Monodora angolensis species. On the other hand, some plant growing in shady and Goniothalamus ridleyi. From that symbiosis, the ants locations will grow slower and with difficulties. An get food, while the plants get protection from pests and example of this in BBG, is one specimen of the species diseases. Weaver ants feeding on leaf-eating caterpillars Orophea hexandra that is growing in the shade of a record in Polyalthia lateriflora and P.rumphii. They help Polyalthia rumphii. plants from pest attacks. Small red ants make a nest in the inflorescence flowers of G. ridleyi. In this interactions are The traits of reproduction suspected ants get nectar and nest, while plant flowers are The reproductive traits of Annonaceae vary according protected by ants from other insect disturbances. However, to the species. According to Handayani (2016) members of symbiosis between these plants species with insect visitors Annonaceae in BBG (40 species) generally, have a still requires further research. According to Frederickson et flowering and fruiting time from January to December. The al (2012), ant-plant interactions are classic examples of numbers of flowering and fruiting species fluctuated each mutualism. Numerous plant species make food or housing month ranging from 29-35 species and 21-28 species to attract ants, which defend the plants against herbivores respectively. The flowering season peaks in October- or other enemies. These ants collect extrafloral nectar or November (35 species), while the peak of the fruiting food bodies from plants. season occurs in December (28 species). The flowering in some species is preceded by a flushing phase while some Research into Annonaceae in Bogor Botanical Gardens do not have a flushing phase. Flushing is a phenomenon in Research is important for revealing potential uses in plants generally initiated by partial or complete fall of adult plants. Research can not be separated from conservation in leaves; followed by growth of new leaves or leaf buds at an institution such as BBG. One of the missions of the the end of the stem, the tip of twigs or axillary leaves; and BBG is to enhance research to support conservation and then followed by the appearance of flowers. From the 40 promote sustainable use of tropical plants resources. The species sampled, indications of flushing were observed in BBG promotes greater of use of Indonesian flora by: 16 species, while 24 species exhibited a"non-flushing" type conducting inventories and evaluation of useful and of flowering. Flowering patterns of the species also vary; potentially useful plant species; by promotion of useful from flowering once a year through to continuous plant species; by conducting ex situ conservation of useful flowering each year. As many as six species flower only and potentially useful plant species; by conducting research once a year, while 24 species flower throughout the year. into the conservation, anatomy, ecology, botany, physiology and horticuture of useful and potentially useful Faunal visitors plant species; and by developing plant collections that have Based on my observation in BBG faunal visitors to potential for public cultivation. These useful plants include Annonaceae plants include insects, squirrels, bats and species with potential to be developed into medicinal birds. Squirrels, bats and birds visit to Annonaceae plants plants, food plants, timber plants, ornamental plants and for eat the fruit of Annonaceae and disperse . There are others. Researchers at BBG are given the option of many visitor insects to Annonaceae flowers, i.e.: black researching and studying selected taxa, e.g. Annonaceae, beetle, bees, fruit fly, green flies, mites, small black ants, Araceae, Arecaceae, Asclepiadaceae, Begoniaceae, small red ants, gray ants, and weaver ants. Direct Nepenthaceae, Orchidaceae, Piperaceae, etc. Various fields observation in BBG, large black beetle visit the flower of of science relating to these taxa are studied, in order to Annona montana. Medium bees, small bees, mites visit the support the development and utilization of plants with flower of Cananga odorata, Dasymaschalon blumei, recognised potential. Some studies relating to Annonaceae Mitrephora polypyrena and Stelechocarpus burahol. Fruit that have been carried out in BBG are presented in Table 2. fly and green fly visit the fruit of Stelechocarpus burahol , Alphonsea teysmannii and Dasymaschalon blumei. Small Seed germination research black ants, small red ants, gray ants, and weaver ants visit The greatest amount of research on Annonaceae in many kinds of species i.e hexapetalus, BBG has concentrated on the processes of seed Goniothalamus ridleyi, Monodora angolensis, Polyalthia germination, followed by reproductive biology. This lateriflora, P. rumphii, P. suberosa, and Stelechocarpus research emphasis is closely related to problem-solving

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Table 2. Research activities on Annonaceae plants that have been germination. This problem generally arises from particular carried out in Bogor Botanic Gardens, West Java, indonesia aspects of the texture or structure of the seed. So, seed anatomy studies have tended to focus on these aspects. Field of Kinds of research Anatomical observation of seeds research showed that Annonaceae seeds have hard texture of the

Anatomy Seeds anatomy of: Artabotrys hexapetalus, ruminate endosperm. This is the factor that causing the Mezzettia parviflora, Platymitra macrocarpa, seeds to take such a long time to germinate (Handayani Meiogyne virgata and Polyalthia suberosa. 2016). According to Svoma (1998), seeds of some Phenology Germination phenology of: Alphonsea members of the Annonaceae have two or three javanica, Annona glabra, A, montana, A. integuments, ruminate endosperm, fibrous mesotesta, and muricata, A. squamosa, Artabotrys imperfect embryo growth at the time the seeds first ripen. hexapetalus, Cananga odorata, Cyathocalyx These factors are suspected as causes of slow or delayed sumatranus, Dasymaschalon blumei, seed germination. The results of seed anatomy research can Meiogyne virgata, Mezzettia parviflora, be used to overcome the problems that exist in seed Mitrephora polypyrena, Orophea hexandra, Platymitra macrocarpa, P.lateriflora, germination of the Annonaceae. P.littoralis, P. rumphii, and P. suberosa. Reproductive Flowering and fruiting time of Annonaceae Reproductive biology research biology species in Bogor Botanic Gardens, Research into the reproductive biology of plants Morphology Seedling morphology of the Annonaceae, growing in BBG is important to an understanding of how flowering morphology of the Annonaceae. best to conserve them. This research attempts to answer Taxonomy of Desmos. such questions as why certain species in the Gardens fail to Propagation Seed propagation, air layering and grafting. flower, or flower but are unfruitful or produce only few Ethnobotany The ornamental plants of Annonaceae, fruit. This research includes observation of the type and potential of Annonaceae. The medicinal plants of the Annonaceae in BBG. number of pollinators, the pattern of blooming, the type and structure of the flowers, the development and maturation of fruit, and aspects of seed germination (Okada 1990, Handayani 2016, Handayani 2017). The research draws upon various scientific disciplines including priorities, to the availability of research materials, and to taxonomy, physiology, phenology, morphology, ecology the amount of research time required to achieve effective and plant propagation technology (Kessler 1988; outcomes. Most of the seeds of Annonaceae in BBG have Nurmawati 2003). BBG conducts research on flowering problems in germination, due to the hardness of the seed and fruiting time of Annonaceae species as a part of this coats, and the immaturity of the embryos when the seeds reproductive biology research program. Particular species first ripen (Handayani 2016). Besides that, seed materials of Annonaceae growing in the Gardens are carefully for many species of Annonaceae become available almost studied as to their time of flowering and fruiting, their every month, so research into germination phenology can flowering types, flowering patterns, fruiting patterns, peak be carried out without delay. Germination phenology flowering times and fruiting seasons, and insect visitors to research focuses on the topics of seed viability, early seed their reproductive parts. The results are utilized for various germination, and seed germination patterns. The result of practical purposes, such as breeding of Annonaceae, this research is very useful for the practical propagation planning exploration trips, collecting Annonaceae seed in and storage of Annonaceae seeds. The seeds of the the wild, ensuring presence of pollinators and adequate Annonaceae are categorized as orthodox seeds (Ellis 1991, pollination, conserving and utilizing the potential of Corsato et al. 2012) if the moisture content of the seeds is Annonaceae species. low, the seeds can be stored for a long time). Some species do not have problems in germination, thus sprouting Ethnobotany research quickly with high germination percentages and vigour, The development and utilization of a plant species is such as Alphonsea javanica, Annona glabra, and part of conservation action (Hidayat et al. 2011; Zegeye Polyalthia lateriflora. Their propagation is usually by using 2017). Botanical gardens explore the potential and seeds. Conversely, species with seeds that germinate utilization of collected species through various sources of slowly with low viability frequently have problems with information about them, such as local people in their native propagation from seed; examples are Meiogyne virgata and localities, user communities, exhibitions, and reviews of Orophea hexandra. Based on germination experiment in published literature. Apart from the botanical gardens BBG, Meiogyne virgata germinate on 50 days after themselves, the results of such research are also utilized by showing, with a viability of 66.67%. Otherwise, Orophea other institutions involved in the plant sciences. For hexandra germinate on 72 days after sowing, with a example, information obtained about plants identified as viability of 66%. potential sources of food can be communicated to other institutions with a particular expertise in the plant food Research on seed anatomy industry. Plants with potential medicinal uses are of interest Research on seed anatomy is carried out on species that to those institutions with a focus on pharmacology and have germination problems, such as slow or delayed developing plant based medicines.The success of these

HANDAYANI – Annonaceae in Bogor Botanical Gardens 597 endeavours depends upon knowledge drawn from various Potential use of Annonaceae collections disciplines such as taxonomy, propagation, biochemistry, Species of the Annonaceae represent a biological and ethnobotany. Taxonomy is useful for accurate resource available to fulfill human needs. Many species in identification of particular plants in the Annonaceae worthy the Annonaceae have been long known for their usefulness to be developed and utilized further. Annonaceae plants are in meeting such needs and many potential new uses are also studied for their use through ethnobotany (Hidayat and being uncovered by ongoing research (Qayed et al. 2015, Astuti 2009; Handayani 2013; Handayani 2014). Ethno- Liaw et al. 2016). Table 3 presents a detailed list of these botanical data is obtained from various sources, such as identified uses for species of the Annonaceae. from local people and from surveys of past written records.

Table 3. List of identified uses for species of the Annonaceae

Genera Species 1 2 3 4 5 6 7 8 9

Alphonsea Alphonsea teysmannii Boerl. + - + ------Alphonsea javanica Scheff. + - + ------Anaxagorea Anaxagorea javanica Blume - - - + - - - - - Annona glabra L. - - - + - - + - - Annona Annona muricata L. + - - + + - + + + Annona montana Macfad. + - - + - - + - - Annona squamosa L. + - - + + - + - - Anomianthus Anomianthus auritus (Blume) Backer + - - - - + - - - Artabotrys Artabotrys hexapetalus (L.f) Bhandari - + - + - + - + - Artabotrys suaveolens (Blume) Blume - + - + - + - - - Cananga Cananga odorata (Lam.) Hook.f. & Thomson - + + + + + + + + Cyathocalyx martabanicus Hook.f. & Thomson - - + - - + - - - Cyathocalyx Cyathocalyx sumatranus Scheff - - + + - - - - + Dasymaschalon Dasymaschalon blumei Finet & Gagnep - - - + - + - - - Desmos Lour - - - + - + - - - Enicosanthum Enicosanthum paradoxum Becc - - + + - - - - - Goniothalamus macrophyllus (Blume) Hook.f. & Thomson - - - + - + - - - Goniothalamus Goniothalamus malayanus Hook.f. & Thomson - - - + - + - - - Meiogyne Meiogyne virgata (Blume) Miq - - + + - - - - - Melodorum Melodorum aberans Maingay ex Hook.f. & Thomson - - - + - - - - + Melodorum fruticosum Lour - - - + + + - - - Mezzettia Mezzettia parviflora Becc - - + + - - - - - Mitrephora celebica Scheff - - + + - + - - - Mitrephora Mitrephora teysmannii Scheff - - + + - - - - - Monodora angolensis Welw - + - + + + - - - Monodora Monodora myristica (Gaertn.) Dunal - + + + + + + - - Monodora tenuifolia Benth - + - + + + + - - Neo-uvaria Neo-uvaria acuminatissima (Miq.) Airy Shaw - - + + - - - - - Orophea Orophea hexandra Blume - - - + - - - - - Polyalthia celebica Miq - - + + - - - - - Polyalthia glauca (Hassk.) Boerl - - + ------Polyalthia Polyalthia lateriflora (Blume) Kurz - - + + + - - Polyalthia rumphii (Blume ex Hensch) Merr - - + + - + - - - Platymitra Platymitra macrocarpa Boerl - - + - - - - - + Popowia Popowia bancana Scheff. - - + + - + - - - Popowia pisocarpa (Blume) Endl. ex Walp. - - + + - - - - - Saccopetalum Saccopetalum horsfieldii Bennett - - + + - + - - - Stelechocarpus Stelechocarpus burahol (Blume) Hook.f. & Thomson + + + + - + - - - Uvaria Uvaria rufa Blume - - - + - - - - - Xylopia Xylopia aethiopica (Dunal) A.Rich. - - + + - - - - -

Note: 1. Fruit, 2. Cosmetic and perfume, 3. Timber, 4. Traditional medicine, 5. Food/beverage industry, 6. Ornamental plants, 7. Insecticide, 8. Ceremonies, 9. Environment control. Source: Sosef et al. (1998), Leboeuf et al. (1982), Wang et al. (2002), Blessing et al. (2010), Bele et al. (2011), Purwantiningsih et al. (2011), Akpabio and Akpapan (2012), Cheng et al. (2012 ), Wang et al. (2012), Eze- Steven et al. (2013), Rosandy et al. (2013), Uyoh et al. (2013), Biba et al. (2014), Enabulele et al. (2014), Tatdao et al. (2014), Handayani (2016), Handayani (2017), Wakhidah et al. (2017)

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Food Table 4. List of genera of Annonaceae with uses for their timber There are eight Annonaceae species in BBG that have or -products (Sosef et al. 1998; Nurfadilah et al. 2017) potential to be used for their edible fruits, either fresh or processed. Annona muricata (soursop) and A. squamosa Genus Wood uses (sweetsop) have potential as fresh fruit producers. They are Alphonsea Construction, ship and boat building, furniture, two of the best known Annonaceous fruits in Indonesia. household utensils, agricultural implements, Both species have been planted on a large scale in fruit tool-handles, packing cases, matches, plantations. Soursop is also used in the food and beverage matchboxes, and firewood. industry. Its fruit are juiced for fresh drinks and packaged Cananga Construction, furniture, tool-handles, wooden beverages. Soursop and sweetsop are also included in shoes, boxes, net floats, making drum, making canoes. various snacks, such as dodol, jam, jelly, and candy.The Cyathocalyx Construction, house building, agricultural fruits of A. muricata are extensively used to prepare syrups, implements, tool-handles, toys, matchboxes, candies, beverages, ice creams and shakes (Moghadamtousi splints, and firewood. et al. 2015). Other species that produce fruits but are rarely Meiogyne Construction, household utensils, furniture, eaten because their taste is less palatable are Annona boxes, plywood, and firewood glabra and A. montana. The pulp of the fruit of Alphonsea Mezzettia Construction, interior finish, packing cases, teysmannii, A. javanica, and Melodorum fruticosum is planking, matchboxes, splints, plywood, and sweet and edible but not commonly consumed. These firewood. edible fruits have high potential to be developed as popular Mitrephora Interior joinery, poles, tool-handles, matches boxes, splints, packing cases, and firewood. local fruits, thus requiring research for their development Polyalthia Construction, house building, furniture, light and domestication. faming, decorative wall paneling, oars, wooden shoes, tool-handles, sporting goods, splints, Cosmetics and perfumes packing cases, boxes, plywood, and firewood. A total of seven species are important as raw materials used for cosmetics and perfumes.Cananga odorata flowers Platymitra Construction, ship and boat building, furniture, (also leaves and fruits) yield an important essential oil sporting goods, agricultural implements, tool- ylang-ylang (contain 1-2% volatile oil) widely used in the handles, packing cases, matchboxes, splint, and manufacture of numerous beauty products such as firewood. Xylopia Construction, interior joinery, packing boxes, perfumes, soap, shampoos and hair oils (Brokl et al. 2013). tool-handles, splints, firewood, matchboxes, Macassar oil is the main product using coconut oil scented and furniture with ylang-ylang oil. This product has been marketed in limited quantity. In Borneo and Java, Cananga odorata flowers are worn in women’s hair to impart an agreeable Ornamental plants scent. An essential oil is extracted from the flowers of The utilization of Annonaceae as ornamental plants is Artabotrys hexapetalus used in perfumes (Shiva et al. well recognized. Ornamental Annonaceae are grouped into 2015). Kept for their fragrant flowers, the fragrance lasts potted plants, landscape plants, hedge plants, and roadside for several days after cutting the flowers. When soaked in trees. Cananga odorata and Artabotrys hexapetalus are water, the flowers are able to scent entire rooms. Another commonly used as potted plants due to their beautiful, popular species used for an oral deodorant and body-odor fragrant flowers. Some members of Annonaceae have remover is kepel fuit or Stelechocarpus burahol (Darusman potential for landscaping, such as Cananga odorata, et al. 2012). According to Tisnadjaja (2006), kepel or Monodora tenuifolia, Artabotrys hexapetalus, burahol fruit has traditionally been used as a perfume Goniothalamus macrophyllus and Dasymaschalon blumei. material, especially in palaces; consuming the fruit can Melodorum fruticosum has potential as a hedge plant. convey its scent to sweat, breath and even urine.The genus Furthermore, Alphonsea teysmannii, Cananga odorata, Monodora produces fragrant flowers. In addition, the flesh Monodora myristica, Polyalthia lateriflora, Mitrephora of its fruit yields essential oils used for perfumes, soaps, polypyrena, and Cyathocalyx martabanicus can be planted and detergents (Eze-Steven et al. 2013), as roadside trees. The diverse shapes and colors of flowers of Annonaceae plant species contribute to their appeal. The Timber flowers of many species have bright and showy petals. Wood is another product that can be obtained from species of Annonaceae. There are 22 species belonging to Traditional medicines 15 genera that have potential use for timber. The wood has Annonaceous plants have been known as sources of potential uses in construction, house-building, ship and traditional medicines since ancient times. However, boat building, furniture, household utensils, agricultural phytochemical and pharmacological research has evolved implements, tool-handles, packing cases, sporting goods, since the discovery of the first acetogenin, uvaricin, in plywood, match boxes, firewood, splints and boxes. Table 1982 (Liaw et al. 2016). Many studies have reported the 4 shows the genera with members that are commonly used presence of chemical compounds in Annonaceae plants that as a source of wood (Sosef et al. 1998; Nurfadilah et al. are useful for medicine (Alali et al. 1999, Wang et al. 2002; 2017). Moghadamtousi et al. 2015). Plants of this family have

HANDAYANI – Annonaceae in Bogor Botanical Gardens 599

recognized sources of alkaloids, diterpenes, flavonoids, and

polyketide compounds. Among them, acetogenins are (%)

regarded as characteristic secondary metabolites of this ies family (Liaw et al. 2016). The Annonaceae acetogenins are now one of the most rapidly growing classes of new natural spec products and offer exciting prospects as anti-cancer, anti- convulsant, anti-arthritic, anti-parasitic, anti-malarial, hepatoprotective, and anti-diabetic agents (Cochrane et al. 2008; Moghadamtousi et al. 2015). Alali et al. (1999) list Percentageof various identified compounds in the Annonaceae as being potentially anthelmintic, in vivo cytotoxic anti-tumorous, Parts of the plant anti-microbial, and anti-protozoal. They recommend Figure 4. Parts of the plants of Annonaceae used in traditional research for new chemotypes as anti-tumor and pesticidal medicines agents (Alali et al. 1999). Based on the listing in Table 3, a total of 40 species belongs to 21 genera have been studied and found to contain chemical compounds useful for medicine.Various brucid (Callosobruchus maculates). Moreover, Monodora plants in the family have been used to treat diseases such as tenuifolia was reported as toxic to the insects, Ootheca cancer, dysentery, fever, diarrhea, mothers’ post-natal mutabilis or cowpea flea beetle (Abdullahi et al. 2010). conditions, itching, ulcer, stomach-ache, worms, Based on the research by Suleiman et al. (2014), the convulsions and constipation (Wang et al. 2002; Blessing essential oil from the leaves of Artabotrys hexapetalus has et al. 2010; Purwantiningsih et al. 2011; Wang et al. 2012; strong activity against female Anopheles gambiae Rosandy et al. 2013; Biba et al. 2014; Enabulele et al. mosquitoes. The repellency activity of essential oil from 2014). The plant part most used for traditional medicine is leaves was higher than from stem bark. the root, followed by the leaves (Figure 4). Leaf utilization for traditional medicine is common in rural communities. Ceremonies According to Nahdi et al. (2016), leaves of Annona Utilization of plants in traditional ceremonies still muricata (soursop) and Stelechocarpus burahol are used by continues today. There are two species of Annonaceae the Turgo, Yogyakarta community for high blood pressure commonly used for traditional ceremonies as well as and in treating gout. The roots, bark, fruit, and leaves of religious ceremonies, Cananga odorata, and Annona Annona muricata are commonly used to treat malaria, muricata. According to Wakhidah et al. (2017), these fevers, liver ailments and headaches among peoples of plants are generally used in ceremonies to welcome the India, Madagascar, Indonesia, Costa Rica, Barbados and a birth of a baby in Nganjuk Regency, in East Java, few countries in Africa and South America (Frausin et al. Indonesia.They are also used in the “Kesada” ceremony 2014). Moghadamtousi et al. (2015) reported that Annona held by Tengger villages in East Java (Pramita et al. 2013; muricata, A. squamosa and A. reticulata are extensively Wakhidah et al. 2017) and the “Oke Sou” ceremony in used as traditional medicines against an array of human West Halmahera, Indonesia (Wakhidah et al. 2017). The ailments and diseases, especially cancer and parasitic "Oke Sou" ceremony is held to give recognition to girls of infections. the community when they reach the age of puberty. Cananga odorata is also commonly used in the “Sura” Pesticides month welcoming ceremony by communities in the There are eight species identified as sources of Nganjuk Regency of East Java (Ayuningtyas and Hakim insecticidal compounds. Isman and Seffrin (2014) reported 2014; Wakhidah et al. 2017). It is also used in the that seed extracts of Annona squamosa and A. muricata can “Sekaten” ceremony in Central Java (Ayuningtyas and be used against the diamond-back moth (Plutella Hakim 2014) and the “Balimau” traditional ceremony in xylostella) and the cabbage looper (Trichoplusia ni). Seed Pariaman, West Sumatra (Hulyati et al. 2014). extracts of A. squamosa also inhibit larval growth of Spodoptera litura. Furthermore, leaves of Annona glabra Habitat for other organisms placed in hen nests kill lice on the fowl (Isman and Seffrin Some species of Annonaceae are used as habitats by 2014). Blessing et al. (2010) stated that infusion of the other organisms (direct observation): examples include leaves is used for treatment of lice, and also for corn pests Cananga odorata, Goniothalamus ridleyi, Melodorum (Spodoptera frugiperda) in Argentina. Another material for fruticosum, Polyalthia lateriflora, P. rumphii and killing larval and pupal of Spodoptera frugiperda is a seed Monodora angolensis. Colonies of weaver ants extract of A. montana (Isman and Seffrin 2014). Cheng et (Oecophylla smaragdina) are commonly found in Cananga al. (2012) reported that the essential oil of Cananga odorata, Melodorum fruticosum, Polyalthia lateriflora, P. odorata leaves is used against maize weevils (Sitophilus rumphii and Monodora angolensis. They complete their zeamais). Abdullahi et al. (2010) reported that African life-cycles on these Annonaceae species. They make a nest nutmeg (Monodora myristica) is effective in controlling by weaving the leaves of the plant. They eat insects that Dermestid maculates infesting dried fish. Seed powders of visit the plant. They breed by laying their eggs in the nest. M. myristica have insecticidal activity against the cowpea

600 BIODIVERSITAS 19 (2): 591-603, March 2018

Another plant used for habitat is Gonioithalamus and P.spathulata (Yusuf et al. 2005). They are important ridleyi. It is a habitat of red ants. The plant and ants are in sources of timber. The presence of illegal logging and land symbiosis. The plant provides an environment and food for clearing for crop cultivation has threatened the ants. Ants keep the plants free from pest attacks. Another sustainability of the species (Yusuf et al 2005). Therefore, example, Cananga odorata, forms a habitat for various ex situ conservation must be carried out to avoid extinction flora and fauna. This tree provides a growing platform and of endangered species of Annonaceae. medium for flora such as pigeon orchids, nest-bird ferns, Conserving representative species of Annonaceae in ant plants, dragon-scale ferns, parasitic plants, and Hoya BBG means that they will be preserved as potential sources spp. of fruit, medicine, ornamentals, insecticides and timber that might benefit humans. It preserves genetic variation in Contributions to environmental health populations and food webs, and for ecosystem services. Plants of the Annonaceae, as components of the BBG Plants with recognized high economic value for production environment, fulfill ecological functions, climatological of fruit, medicines, ornamentals, insecticides or timber tend functions, and hydrological functions. These functions to be widely developed, but those with low economic value contribute to the health of the environment both within and or unrecognized value will not be cultivated and will be beyond the BBG precinct. Examples of the ecological more likely to be cut down. Annona muricata and A. functions to which they contribute are in regulating squamosa are fruit-producing plants well known to the temperature, humidity, and water reserves in Bogor. BBG public. These species are widely grown both individually is often called the "lungs of Bogor City". All plants in BBG and in plantation. However, other species, such as Annona absorb carbon dioxide and release oxygen into the air. The glabra, A. montana, Alphonsea teysmanii, A. javanica, and ability of plants to generate oxygen and to transpire water Stelechocarpus burahol, have fruits with low economic from their leaves is an example of their climatological role. value and are rarely planted or are even cut down by the The density of the human population and vehicle traffic in community (Tisnadjaja et al. 2006). The use of Bogor affects the quality of the urban environment of Annonaceae plants for traditional medicine is widespread. Bogor city.Various human activities release carbon dioxide As a result, some people still take plants or their parts into the atmosphere in ever-increasing amounts. Plant life, directly from the forest. If this exploitation continues, it can on the other hand, including BBG’s significant Annonaceae decrease the plant population leading to their extinction. collection, absorbs carbon dioxide. Although almost all The harvest of root and bark for medicine can lead to plant species function as “carbon sinks”, large growing eventual death of the plants. Another threat is the logging trees like Cananga odorata, Annona squamosa and A. of Annonaceae plants as a source of wood. muricata are considered particularly effective carbon sinks Annonaceae plants are also a source of germplasm for (Usmadi, pers. comm.). BBG also serves a hydrological ornamental plants. Pressure on forests, exploitation of function, to which the Annonaceae contribute, by potential ornamental plants, and trade in ornamental plants intercepting rainfall and facilitating its infiltration into the of high value or even of low economic value have soil. threatened their populations in forests (Nagel 2011). Therefore, specimens of potential ornamental plants need Why is conservation of Annonaceae important? to be preserved in safe locations outside their natural The occurrence of large-scale natural habitat habitat. If such a species is planted in BBG, and later on the destruction is a key reason why active steps are required to species is lost from its natural habitat, then it is often preserve plant diversity. The conversion of natural habitat possible to return preserved specimens to the place where into land for housing, industry, agriculture, and plantations the plant originated. Some Annonaceae plants are endangers the continuing existence of some plant species, important sources of insecticidal compounds. Research on including particular members of the Annonaceae (Yusuf et the chemical the composition of such potential insecticidal al. 2005; Komara et al. 2016).The rate of forest destruction plant species should be developed in order to reduce as natural habitat, world-wide, has been so rapid in recent dependence on chemical insecticides. Annonaceae species decades that preservation efforts have scarcely been with potential as sources of biological insecticides should adequate to reduce the rate of species loss (Yusuf et al. be preserved ex-situ in locations like BBG. 2005, Komara et al. 2016, Zegeye 2017). Although in situ Annonaceae plants need to be preserved as important conservation is already an important part of conservation components of the BBG ecosystem, in its role as the "lungs strategies in Indonesia, this is not specifically aimed at of Bogor city" benefiting human health and stabilizing the preserving the Annonaceae. According to Komara et al. microclimate of the local environment. Annonaceae plants (2016), the production forest of East Kutai, East provide feed and shelter for local fauna such as birds, Kalimantan province is used as a mining area. In this area, squirrels, bats, pollinators, and beneficial insects. the species Neo-uvaria acuminatissima, Polyalthia obliqua, Annonaceae trees also provide habitat for other flora, such Polyalthia sumatrana and Sageraea glabra have been as ferns, orchids, lichens and other epiphytes. The loss of eliminated. Another example of threatened Annonaceae Annonaceae would harm the survival of some of these sustainability in nature is apparent in West Sumatra. The dependent species. Observation in BBG, when the natural forest of Rimbo Panti in West Sumatra has long Annonaceae plants die, plants that stick will also die. been a habitat for Cyathocalyx sumatranus, Meiogyne Conservation of Annonaceae in BBG is also for historical virgata, Mitrephora sp, Polyalthia obliqua, P. reticulata reasons. Some Annonaceae specimens are old plants well

HANDAYANI – Annonaceae in Bogor Botanical Gardens 601 over 100 years of age. Based on the author’s observations, needed. Weeding is carried out to remove competitive many of these old species in the collection have long weeds around the plant, as well as to loosen the soil around played an important role in the forest ecosystem of BBG; the plants. This can stimulate better root growth. examples include Alphonsea teysmannii, Cyathocalyx Fertilization is done at the beginning of planting and/or martabanicus, Mezzettia parviflora, Platymitra during the plant’s growth period. Fertilizer used is compost, macrocarpa and Stelechocarpus burahol. They are big manure or inorganic fertilizer. Pruning is usually carried trees with significant ground coverage, providing habitat out on branches that are too dense. Plants with canopies both underground and in their crowns for other living that are too thick can disrupt the surrounding plants. things. Platymitra macrocarpa planted in 1844 is the oldest Pruning aims to facilitate sunlight reaching the soil surface, living Annonaceae tree in the Gardens. This plant is a to avoid fungal attack, and to prevent trees falling over living type specimen, so it has great taxonomic trees during strong winds. The eradication of pests and significance. According to Kessler (1988), this species is diseases is carried out on affected plants, by spraying both distributed very locally and seems to be rare.Old trees have biological and chemical pesticides. high conservation value, especially if the species to which Because of its function as a center of acclimatization, they belong no longer survive in nature or are difficult to plant display, conservation, and research (physiology, find. morphology, taxonomy, germination, etc.), BBG also Some members of Annonaceae also have historical carries out propagation of plants held in its collection. value as flora of provincial identity in Indonesia.Cananga Propagation by vegetative or generative means is carried odorata is the of North Sumatra Province, out either conventionally or by tissue culture, especially for while Stelechocarpus burahol is the floral emblem of rare plants, endemic plants, critical plants (i.e., plants for Yogyakarta Province. Melodorum fruticosum is the which there is only one collection) and some ornamental national flower of Cambodia. It is also the provincial plants. The results of these propagation efforts are used to flower of Sisaket Province, in Thailand. replace dead plants, to plant displays, for landscaping, to provide research materials, for use in community service, How does Bogor Botanic Gardens conserve plants of the and for environmental education. Annonaceae family? In summary, the present study has summarised the Exploration, cultivation, research, utilization, and diversity of the family Annonaceae growing in the BBG in dissemination of information are all part of BBG’s program terms of plant species; plants origins; habit; age of plants of plant conservation. The plant collection in the Gardens growing in the Gardens; growth sites; their reproductive comes from forest directly, from donations, and from seed traits; their young leaf color; and flower color. Species of exchange with other institutions. BBG carries out Annonaceae have been listed that have potential uses for exploration throughout the archipelago to collect plants providing fresh fruit; cosmetics and perfumes; timber; from the forest, especially of rare, endangered and traditional medicines; processed foods and beverages; potentially useful plant species. They collect seedlings, ornamental plants; insecticides; habitat for other dependent cuttings, fruit or seed. Selected materials are then recorded: organisms; and for benefits to the local environment. collector codes, date of collection, species name, genus Destruction to Annonaceae native habitats means that ex name, family name, geographic coordinates and altitude of situ conservation of Annonaceae is an important part of the location, habitat environment details, type and quantity of BBG mandate. Many species of Annonaceae in BBG are of materials taken, are all recorded. Data obtained from the high historical value. To support ex situ conservation, BBG exploration site are submitted to the Nursery and researches the anatomy, phenology, reproductive biology, Registration section of BBG. Plants collected from natural morphology, taxonomy, propagation technology and field sites are first acclimatized and adapted in a nursery. ethnobotany of Annonaceae. In support of its conservation After a plant reaches a height of 50-100 cm it is planted out program, BBG carries out exploration, cultivation, in the Gardens. The plant is given a name plate made of research, utilization, and dissemination of information. zinc. Each plant is given a name plate which bears the name of the species, family, plant origin and planting location. If the name of the species is unknown, it is just ACKNOWLEDGEMENTS labelled with name of the family and genus. For healthy growth of a collection, it is necessary to The author would like to thank the BBG exploration carry out intensive maintenance by applying appropriate team for collecting Annonaceae within the Indonesian cultivation technology.This involves preparing a suitable archipelago. I also wish to thank Dr. Graham Eagleton for area of ground and planting hole, selecting a healthy helpful discussion and comments on the manuscript’s seedling, watering, weeding, fertilizing, pruning, and English. controlling pests and diseases. A planting hole is dug 2-3 weeks before planting. In the hole is placed a mixed planting medium of soil, husk, compost, and manure. REFERENCES Selected plantlets must be lush, healthy, and strong at the time of planting and have no signs of pests or Abdullahi N, Auwal F, Yusha’u M, Bello B. 2010. 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